The largest arboreal and terrestrial frugivore in the Neotropics: the muriqui ( Brachyteles arachnoides ) (A) and the tapir ( Tapirus terrestris ) (B). Photos by Pedro Jordano and Mauro Galetti, respectively. doi:10.1371/journal.pone.0056252.g001 

The largest arboreal and terrestrial frugivore in the Neotropics: the muriqui ( Brachyteles arachnoides ) (A) and the tapir ( Tapirus terrestris ) (B). Photos by Pedro Jordano and Mauro Galetti, respectively. doi:10.1371/journal.pone.0056252.g001 

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Functional redundancy has been debated largely in ecology and conservation, yet we lack detailed empirical studies on the roles of functionally similar species in ecosystem function. Large bodied frugivores may disperse similar plant species and have strong impact on plant recruitment in tropical forests. The two largest frugivores in the neotropic...

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... has been hypothesized that in biodiversity-rich ecosystems, the extinction of some species will not cause a substantial loss in ecosystem function if remnant species play equivalent roles and are capable of taking over the functions played by extinct species (i.e. functional redundancy) [1]. Analysis of the seed dispersal network in tropical forests shows high connectedness and diet overlap among several species and groups of vertebrates [2], suggesting high redundancy in the system. The selective and relatively fast removal in the diversity and biomass of large-bodied vertebrates, a phenomenon named ‘‘defaunation’’ [3], is creating shifts in vertebrate communities often dominated now by few small-bodied species [4,5], with potential changes in their functional diversity in the vertebrate communities. Erosion of functional diversity via defaunation may ultimately affect differently the recruitment of plant species, depending on functional traits such as fruit and seed sizes [6,7,8,9]. Large vertebrates are particularly important, because they remove a larger amount of seeds, disperse them for longer distances, and are able to disperse larger seeds than smaller frugivores [10,11,12,13]. Primates play an important role in forest dynamics, as they are the largest arboreal forest frugivores and constitute 25%–40% of the frugivore biomass in most tropical forests [14]. Ateline primates (e.g. Ateles, Brachyteles, Logothrix ), for instance, can disperse millions of seeds per year [15], and thanks to their wide variety of feeding behaviors, they create different seed shadows and dispersal kernels [11,16]. Another important fruit- eating group in the neotropics is large ungulates, such as peccaries, deer and tapirs, which comprises the largest extant frugivores in tropical forests. While peccaries and deer are most seed predators, tapirs ( Tapirus spp.) eat large amounts of fruits, disperse large quantities of seeds, often at long distances, and are able to disperse very large seeds even across heavily disturbed areas [17,18,19]. These megafrugivores are amongst the most hunted animals in the neotropics. For instance every year about 47,000 tapirs and 700,000 ateline monkeys are killed in the Amazon forest for subsistence [20]. The situation is no better in the Atlantic forest, where only 12% of the original forest is left [21] and hunting is still widespread [22]. Neotropical rainforests may be particularly sensitive to the removal of frugivores because between 40% and 90% of woody species bear fleshy fruits dispersed by vertebrates [23]. Although seed dispersal by primates and ungulates has been widely studied in terms of seed dispersal [24,25,26], we lack comparative studies on seed dispersal effectiveness between co-occurring large-bodied species. Are the largest megafrugivores, tapirs and ateline primates, redundant or complementary seed dispersers? This question is particularly important if we want to predict the impact of defaunation on plant recruitment [27] and ecosystem function. Here we compare the seed dispersal effectiveness of the largest remaining arboreal and terrestrial frugivores in the Neotropical forests, the muriqui ( Brachyteles arachnoides ) and the tapir ( Tapirus terrestris ) (Figure 1). This study was carried out at Carlos Botelho State Park (hereafter CBSP), a 37,644 ha Protected Area in a continuous massif named ‘‘Serra de Paranapiacaba’’ in S ̃o Paulo state, southeastern Brazil (24 u 44 9 S, 47 u 44 9 W; Figure 2). The topography is hilly, with slopes ranging from 10 u up to 50 u degrees, and very few flat tracts, usually along larger rivers. There is a high altitudinal variation inside CBSP, ranging from 30 m to 1100 m a.s.l. Average rainfall is about 2,000 mm/year, with no clear dry season and mean temperature is 20 u C. The vegetation is Ombrophilous Dense Atlantic Forest, ranging from lowland to montane physiognomy [28]. More than 1151 species of woody plants have been recorded, with the most abundant families represented by Myrtaceae, Arecaceae, Lauraceae, Rubiaceae, Sapotaceae and Moraceae [29]. The landscape around the park is dominated by monocultures of Pinus and Eucalyptus , pastures, and other small-scale agricultural crops. The Paranapiacaba massif comprises more than 120,000 ha of Atlantic Forest distributed through four protected parks and several private properties and holds an almost complete assemblage of threatened mammals, including jaguars ( Panthera onca ), bush dogs ( Speothos venaticus ), tapirs ( Tapirus terrestris ) and muriquis ( Brachyteles arachnoides ), although white-lipped peccaries ( Tayassu pecari ) are locally extinct [22,30]. Specifically, our study was conducted in the home range of a group of 35 southern muriquis Brachyteles arachnoides (hereafter muriquis), corresponding to approximately 850 ha at about 750 m a.s.l, located at the extreme north of CBSP [31] (Figure 2). From April 2008 to July 2009, we searched for tapir feces by walking along a grid of existing trails and also following tapirs tracks distributed throughout the study area, totaling 198 km walked, with an average of 14 km per month. The effort was distributed in such a way that all topographic features (small rivers, dry valleys, slope and top hill) were sampled in equal proportions. We defined as ‘‘latrine’’ a clump of tapir feces with different ages inside a 5-meter radius [25]. The latrines were visited monthly and we collected dispersed seeds in one third of the whole fecal material in order to not interfere in the use of the latrine, so to quantify the seed dispersal we multiplied the results of the analyzed samples by three. During the same period, we followed individuals of the sub- groups of muriquis habituated to human presence, from sunrise (5:15 h) to sunset (18:30 h) totaling 246,7 km walked with an average of 17,5 km per month. Observations totaled 432 h of direct contact, of which 382 h (89%) were on adults. We totaled 31 complete days of observation following the same sub-group from sunrise (waking-up site) to sunset (sleeping site) and 20 incomplete days (i.e. observation interrupted for more than 1 hour). To verify the sub-group size we collected data on the number of muriquis surrounding the focal individual (about 15 m) three times a day (8:00, 12:00 and 16:00). Points along daily routes were geopositioned every 15 minutes. To determine the feces deposition pattern, each observed defecation event, here defined as a defecation of a single individual at the same place within 1 minute, was also geopositioned. The deposition pattern was defined as ‘‘clumped’’ if the feces fell in less than 30 cm radius, or ‘‘scattered’’ if, while falling, the feces collided with the leaves and branches of the understory and reached the ground in more than 30 cm radius [26]. Muriqui and tapir feces were collected and analyzed in the laboratory. When tapir feces were located in water we only collected them if the boluses were whole (i.e. not broken or dissolved). For all samples, we recorded the topographical feature (water, dry valley, slope or hilltop), distance (m) from the nearest tree with DBH . 40 cm and all possible parental fruiting trees in an area of 25 m radius. All feces were sieved through a mesh of 2 6 2 mm and all remaining seeds were identified with the aid of guides [32] and by comparing with a collection of voucher specimens. Seeds were also counted, measured with digital calipers with 0.01 mm precision and classified as ‘‘predated’’ if broken or chewed or ‘‘non predated’’ if no damage was observed [33]. The seeds # 2 mm (e.g. Coussapoa sp.) were collected in a plate under the sieve and whenever possible were identified and the number of seeds estimated. We also collected fallen fruits under fruiting trees, removed the pulp and measured the seeds for comparison with dispersed seeds. To estimate the minimum seeds dispersed by month by muriquis we used the average of 30.6 seeds dispersed by day, obtained from five complete days where we were able to collect at least 4 defecation of the same individual (R. S. Bueno, unpublished data) and multiplied by 30 days. For tapirs, we used the average of 140 seeds per individual per month. This was based on the number ...

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... Some estimates posit that hunting-driven defaunation affects a greater area of tropical forests than logging and fragmentation combined (Benítez-López et al., 2019;Harrison et al., 2016;Pires & Galetti, 2023). Despite the ubiquity of defaunation, it remains unclear (1) the extent to which animals remaining in defaunated forests compensate for interactions and services previously performed by the larger extirpated species and (2) the functional outcomes of these altered or lost interactions (Bueno et al., 2013;Culot et al., 2017;Fricke et al., 2018;Sekar & Sukumar, 2013). Developing nuanced insight into how defaunation per seimpacts ecological processes is an important step to understanding the consequences of anthropogenic change in tropical forests. ...
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Anthropogenic pressures such as hunting are increasingly driving the localized functional extinctions of all or most large and medium-sized wildlife species in tropical forests, a phenomenon broadly termed defaunation. Concurrently in these areas, smaller-bodied wildlife species benefit from factors such as competitive release and experience population increases. This transformation of the wildlife community can impact species interactions and ecosystem services such as seed dispersal and seed-mediated geneflow with far reaching consequences. Evidence for negative genetic effects following defaunation is well-documented in large-seeded plants that require large frugivores for long distance seed dispersal. However, how defaunation affects small-seeded (< 1.5cm diameter) plants, which are dispersed by frugivores with a wide range of body-sizes and responses to anthropogenic threats, is not well understood. To better understand the reach of defaunation’s impacts on tropical plant communities, we investigated spatial and genetic patterns in a hyperabundant small-seeded palm, Euterpe precatoria in three sites representing distinct defaunation levels. We found significantly higher fine-scale spatial genetic structure among nearest-neighbor seedlings in the defaunated site and in the recovering, partially defaunated site relative to the faunally-intact site. Defaunation was associated with shorter distances between seedlings and adults and lower genetic distance between adult and seedling cohorts. No effects were detected on inbreeding and genetic diversity; however, we caution that trends we detected indicate that defaunation influences the spatial distribution of genetic variation even in small-seeded plants that inherently have a broad suite of seed dispersal agents, and this could lead to negative downstream effects on genetic diversity.
... The lowland tapir (Tapirus terrestris, hereafter referred to as "tapir") is a large terrestrial neotropical herbivore with a broad diet, feeding on many different plant species and sources such as fruits and seeds of varying sizes (Fragoso and Huffman, 2000;Naranjo, 2018;Paolucci et al., 2019) and have been reported to consume fruits from 194 plant species in the Neotropical region (Hibert et al., 2011). Tapirs are also known to be effective seed disperser agents for palms (Fragoso et al., 2003) and many other fruiting plant species (Bueno et al., 2013). Tapirs are communal latrine defecators that deposit large amounts of dung in the same location (Fragoso, 1997;Tófoli, 2006). ...
... The CBSP is also home to many animal species, including around 330 bird species (Antunes et al., 2013), 65 amphibian species, 59 reptile species (Forlani et al., 2010), and 53 non-flying mammal species (Brocardo et al., 2012). Our study was conducted in an 850-hectare region located at the extreme north end of the CBSP, where previous site visits had indicated a high probability of finding tapir latrines (Bueno et al., 2013) (Fig. 1). ...
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Foraging is essential for animal survival, as it provides the nutritional resources to sustain metabolism and all activities that animals undertake. Communal latrines are sites where multiple individuals of the same species defecate and can have multiple functions. Latrine behavior has been recorded in many animal species, including lowland tapirs (Tapirus terrestris), which consume a wide variety of plants and fruits and defecate large piles of dung, sometimes containing many seeds. Due to the concentration of seeds and other defecated material, latrines may thus serve as direct sources of food for other vertebrates, including insectivores feeding on invertebrates attracted to dung. Here, we studied which vertebrate animals were recorded foraging in tapir latrines, how long they spent foraging on latrines, and how their foraging behavior varied with the time of day and days since tapir defecation. Since tapirs are generalist foragers with a large diet breadth, we expected that their feces might attract vertebrate foragers with a variety of dietary habits (e.g., frugivores, granivores, omnivores, insectivores) in distinct foraging periods within a day. We also expected that the foraging events would be greatest in the days immediately following tapir defecation. We monitored 27 tapir latrines with camera traps for six months, recording foraging vs. non-foraging behaviors. We observed nine vertebrate species foraging in tapir latrines with five frequent foragers: the frugivores Guerlinguetus brasiliensis (50% of total foraging records) and Tinamus solitarius (16%, also a granivore) and the omnivores Turdus albi-collis (18%), Chamaeza campanisona (10%) and Odontophorus capueira (6%). Foraging and non-foraging events throughout the day differed significantly for G. brasiliensis (p= 0.006), T. solitarius (p= 0.01), and C. campanisona (p= 0.001), and all species were diurnal, foraging between 05:00 h and 18:00 h. The foraging probability of C. campanisona and T. albicollis was affected by the time lapse since tapir defecation. Our study highlights that communal latrines such as those maintained by lowland tapirs can be an important resource supply for some 2 vertebrate consumers with different diets and could contribute to maintaining diversity in tropical forests. We call for future studies to inspect the importance of latrines as foraging sites for other species and ecosystems.
... Human-induced changes affect mostly large-bodied animals that rely on large home ranges, and impact their role in habitat maintenance and ecological processes, such as seed dispersal (Cordeiro and Howe 2003;Galetti and Dirzo 2013). In the Atlantic Forest, the lowland tapir and the muriqui are the largest frugivorous mammals occupying large home ranges, and are the species able to carry the largest seeds (Fragoso and Huffman 2000;Bueno et al. 2013). Large-seeded species are of particular importance because they contribute significantly to carbon storage, which helps to regulate the level of carbon dioxide in the atmosphere (Peres et al. 2016;Bello et al. 2021). ...
... Large-seeded species are of particular importance because they contribute significantly to carbon storage, which helps to regulate the level of carbon dioxide in the atmosphere (Peres et al. 2016;Bello et al. 2021). However, although both tapirs and muriquis are large frugivores, they play complementary roles, as the species of plants and quantity and spatial distribution of the seeds that they disperse differ (Bueno et al. 2013). In addition, the probability of seed burial by dung beetles, seed predation, and survival of the seeds that tapirs and muriquis disperse differ (Lugon et al. 2017). ...
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The dispersal of large-seeded species strongly depends on medium-sized and large frugivores, such as primates, which are highly susceptible to population declines. In the Atlantic Forest, brown howler monkeys Alouatta guariba are medium-sized folivorous-frugivorous species that are likely to occur in small to large fragments where the largest frugivores are extinct. However, populations of this primate have been suffering from forest fragmentation, habitat loss, hunting, and the direct and indirect effects of yellow fever outbreaks, which increase the importance of understanding their role as seed dispersers and the impacts of their potential loss. The richness and abundance of large-seeded species might also be reduced in smaller fragments, which could directly affect the magnitude of the potential impact of disperser extinction on plant recruitment. Here, we tested the following mutually exclusive predictions on the effect of fragment size on plant richness and relative density of medium- and large-seeded species consumed by brown howler monkeys in fragments smaller than 1500 ha: the number and the relative density of plant species potentially affected by the local extinction of these monkeys will be (1) directly related to forest fragment size, or (2) not related to forest fragment size. Plant richness and the relative density of large- and medium-sized seed species consumed by brown howler monkeys did not vary with fragment size, corroborating our second prediction. Thus, the local extinction of brown howler monkeys would have a similar potentially negative impact on plant regeneration for the range of tested fragment sizes. We discuss the limitations of our results and suggest other lines of enquiry for the refinement of our conclusions.
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... The CBSP is also home to many animal species, including around 330 bird species (Antunes et al., 2013), 65 amphibian species, 59 reptile species (Forlani et al., 2010), and 53 non-flying mammal species (Brocardo et al., 2012). Our study was conducted in an 850-hectare region located at the extreme north end of the CBSP, where previous site visits had indicated a high probability of finding tapir latrines (Bueno et al., 2013) (Fig. 1). ...
... It provides a greater amount of habitat and enables greater availability of resources for the occurrence of L. chrysomelas, in addition to maintaining larger populations in these areas. The dispersal of primates between closer fragments also reduces the risk of predation to which these species are exposed to (Bueno et al., 2013;Moraes et al., 2018). Therefore, we emphasize the importance of cabrucas in contributing to the functional connectivity of the landscape in the eastern portion of the geographic range of L. chrysomelas, which can facilitate animals dispersal and reduce their risk of predation. ...
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The golden‐headed lion tamarin ( Leontopithecus chrysomelas ) is an endangered primate that occurs exclusively in the Atlantic Forest of southern Bahia, Brazil. Its geographic range has been severely reduced by deforestation and its populations are restricted to a human‐modified landscape consisting primarily of Atlantic forest fragments and shade cacao ( Theobroma cacao ) agroforestry, locally known as cabrucas . In the last 30 years, there has been a 42% reduction in the geographic range and a 60% reduction in the population size of L. chrysomelas , with only 8% of its habitat represented by protected areas. Thus, we investigated the occurrence of L. chrysomelas in forest fragments and cabrucas based on interviews and using playback census, and evaluated the influence of landscape attributes on its occurrence. The occurrence was measured using a Generalized Linear Model using a set of 12 predictor variables, including fragment size and elevation. L. chrysomelas inhabited 186 (38%) of the 495 forest fragments and cabrucas . Most inhabited habitat patches ( n = 169, 91%) are in the eastern portion (ca. 70 km wide region from the Atlantic coast to inland) of its geographic range. The remaining ( n = 17, 9%) are in the western portion of the distribution, between 70 and 150 km from the Atlantic coast. Our models indicate a higher occurrence of L. chrysomelas in the eastern portion of its geographic range, where the landscape exhibits lower land cover diversity, greater functional connectivity, lower altitudes (<400 m), and is primarily composed of forest fragments and cabrucas with a higher core percentage. In contrast, we observed a lower occurrence of L. chrysomelas in the western portion, where the landscape is more diverse and heterogeneous due to anthropogenic activities, such as agriculture and livestock. We urge the establishment of ecological corridors via reforestation of degraded areas in the western portion of the range. This increase in habitat availability and suitability in the west together with the protection of the forests and cabrucas in the east would increase our chances of saving L. chrysomelas from extinction.
... In contrast, a study in Amazonian Peru (Paine & Beck, 2007) found that excluding large terrestrial herbivores did not affect seedling recruitment. In Amazonian sites in Brazil, white-lipped peccaries, which have a different home range and group size from collared peccaries (Akkawi et al., 2020;Bodmer, 1990) increased seedling density, but tapirs did not , despite being a relict megafauna species know to consume a remarkable number of seed species (355) in tropical forests (Bueno et al., 2013;Fragoso et al., 2003). Differences between the Costa Rican and Amazonian sites, including more species of terrestrial herbivores, likely owing to the largely intact populations of top predators in the Amazonian site (Rocha-Mendes et al., 2010;TEAM Network, 2020;Voss & Emmons, 1996) as well as potential differences in plant community characteristics (e.g. ...
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... Primates are one of the most seriously threatened animal groups in tropical areas, mainly due to habitat loss, deforestation, and fragmentation (Stevenson 2016;Brum et al. 2017;Roncancio et al. 2010;Bueno et al. 2013;Rattis et al. 2018). They play central ecological roles in ecosystems as dispersers, pollinators, predators, and prey. ...
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One of the fundamental objectives of ecology is to study the relative importance of ecological, evolutionary, and stochastic processes in determining local community structure. Many studies have focused on taxonomic diversity, paying relatively little attention to other dimensions of biological diversity, such as phylogenetic and functional diversity. Little is known about how these dimensions relate to each other, and the ecological processes that influence their variation. In this study, we characterize these three dimensions of biodiversity in 14 primate communities from different ecosystems in Ecuador to understand possible mechanisms responsible for their assembly. Results show that coastal communities are taxonomically less diverse than those from the Amazon and present different functional groups. On the other hand, phylogenetic diversity is higher in Amazonian communities, showing a tendency for overdispersion (high values of MPD PD = mean phyloge-netic distance per pair and low PSC = degree to which coexisting species are related). This indicates a possible influence of biological factors, such as competition, on community assembly. For all three dimensions, climatic variables were the most significant predictors of community structure, while vertical forest structure contributed significantly to variation in the phylogenetic dimension. The high functional diversity reported in this study highlights the importance and vulnerability of this group and the ecosystems they inhabit. Macroecological studies, such as the one presented here, allow a better understanding of community structure and provide important information for the development of conservation strategies.
... Therefore, dietary preferences of animals and cryptic functional loss of interactions, rather than morphological mismatches 76 , can be expected to limit the ability of the remaining species to compensate interactions after the loss of common species in our study system. Moreover, the loss of certain animals could affect population processes that are beyond the scope of this study, for instance range expansion 32,88 , gene flow 89 , and plant migration in response to climate change 17,18 . ...
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Mutualistic interactions are by definition beneficial for each contributing partner. However, it is insufficiently understood how mutualistic interactions influence partners throughout their lives. Here, we used animal species-explicit, microhabitat-structured integral projection models to quantify the effect of seed dispersal by 20 animal species on the full life cycle of the tree Frangula alnus in Białowieża Forest, Eastern Poland. Our analysis showed that animal seed dispersal increased population growth by 2.5%. The effectiveness of animals as seed dispersers was strongly related to the interaction frequency but not the quality of seed dispersal. Consequently, the projected population decline due to simulated species extinction was driven by the loss of common rather than rare mutualist species. Our results support the notion that frequently interacting mutualists contribute most to the persistence of the populations of their partners, underscoring the role of common species for ecosystem functioning and nature conservation.
... At the ecological level, functional equivalence can be considered in which multiple species can share similar, or even identical, roles in an ecosystem [61]. Several examples of this type of redundancy in the complex systems, from plant-pollinator relationships [62] to plant-animal seed dispersal mechanisms [63] can be mentioned. In structural engineering, heretofore, no classification referring to the involved mechanisms is suggested. ...
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Bio-inspired solutions are widely adopted in different engineering disciplines. However, in structural engineering, these solutions are mainly limited to bio-inspired forms, shapes, and materials. Nature is almost completely neglected as a source of structural design philosophy. This study lists and discusses several bio-inspired solutions classified into two main classes, i.e., compartmentalization and complexity, for structural robustness design. Different examples are provided and mechanisms are categorized and discussed in detail. Some provided ideas are already used in the current structural engineering research and practice, usually without focus on their bio-analogy. These solutions are revisited and scrutinized from a bio-inspired point of view, and new aspects and possible improvements are suggested. Moreover, novel bio-inspired concepts including delayed compartmentalization, active compartmentalization, compartmentalization in intact parts, and structural complexity are also propounded for structural design under extreme loading conditions.
... Seed dispersal is fundamentally important for determining the spatial and genetic structure of plant populations (Dick et al., 2008;Voigt et al., 2009) and in ensuring their long-term ability to adapt to change (Corlett & Westcott, 2013;McConkey et al., 2012). In tropical forests, most seeds are dispersed by animals (Howe & Smallwood, 1982) which vary widely in their fruit selection and their seed dispersal capabilities (Bueno et al., 2013;Martínez et al., 2008). Determining how these communities of diverse seeddispersing animals are structured is essential for understanding the relative roles and potential importance of different animal species in seed dispersal, which is helpful to predict the resilience of ecosystems to the various disturbances that impact them (Fricke et al., 2017;Garcia et al., 2013;Markl et al., 2012). ...
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Southeast Asia is a conservation priority region due to its high biodiversity—including megafauna—and high rates of defaunation, which has negative impacts on key ecological processes such as seed dispersal. Yet, seed dispersal interactions at the community level have rarely been described in this region. This is a major knowledge gap because medium‐size and large animals are disproportionately affected by defaunation and they also have critical roles as seed dispersers. Hence, community‐wide studies that encompass a full range of animal body sizes across diverse regions are required, to enable an improved understanding of defaunation impacts. Here, we (a) describe a highly diverse Southeast Asian seed dispersal network (Khao Yai National Park, Thailand), (b) assess the role of body size in identifying important animals and (c) determine if threatened species are disproportionately important in the network. The network is highly nested and modular, with species phylogeny, body size and seed size having a major influence on modularity; mammals and birds occupied different modules. Generalist species playing important roles in the network were mainly medium or large‐sized. However, the largest disperser (elephants) played a relatively minor role in seed dispersal in this community, and bulbuls were important despite their small size. Many threatened animal species were important within the network as connector species and through their interactions with a larger number of plant species. Consequently, the resilience of this biodiversity hotspot is at threat by the potential nonrandom loss of the most important seed dispersers.